Cardiopulmonar y Imaging • Original Research

Bartykowszki et al.
Quality of Coronary CTA Images of HTx Recipients

Cardiopulmonary Imaging
Original Research

Image Quality of Prospectively

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ECG-Triggered Coronary
CT Angiography in Heart
Transplant Recipients
Andrea Bartykowszki1 OBJECTIVE. Cardiac allograft vasculopathy (CAV) is among the top causes of death 1
Márton Kolossváry 1 year after heart transplantation (HTx). Coronary CT angiography (CTA) is a potential alter-
Ádám Levente Jermendy 1 native to invasive imaging in the diagnosis of CAV. However, the higher heart rate (HR) of
Júlia Karády 1 HTx recipients prompts the use of retrospective ECG-gating, which is associated with higher
Bálint Szilveszter 1 radiation dose, a major concern in this patient population. Therefore, we sought to evaluate
the feasibility and image quality of low-radiation-dose prospectively ECG-triggered coronary
Mihály Károlyi1
CTA in HTx recipients.
Orsolya Balogh2 MATERIALS AND METHODS. In total, 1270 coronary segments were evaluated in
Balázs Sax1 50 HTx recipients and 50 matched control subjects who did not undergo HTx. The control
Béla Merkely 1 subjects were selected from our clinical database and were matched for age, sex, body mass
Pál Maurovich-Horvat 1 index, HR, and coronary dominance. Scans were performed using 256-MDCT with prospec-
tive ECG-triggering. The degree of motion artifacts was evaluated on a per-segment basis on
Bartykowszki A, Kolossváry M, Jermendy AL, et al.
a 4-point Likert-type scale.
RESULTS. The median HR was 74.0 beats/min (interquartile range [IQR], 67.8–79.3
beats/min) in the HTx group and 73.0 beats/min (IQR, 68.5–80.0 beats/min) in the matched
control group (p = 0.58). In the HTx group, more segments had diagnostic image quality com-
pared with the control group (624/662 [94.3%] vs 504/608 [82.9%]; p < 0.001). The mean ef-
fective radiation dose was low in both groups (3.7 mSv [IQR, 2.4–4.3 mSv] in the HTx group
Keywords: coronary CT angiography, heart
vs 4.3 mSv [IQR, 2.6–4.3 mSv] in the control group; p = 0.24).
­transplantation, image quality
CONCLUSION. Prospectively ECG-triggered coronary CTA examinations of HTx re-
doi.org/10.2214/AJR.17.18546 cipients yielded diagnostic image quality with low radiation dose. Coronary CTA is a prom-
ising noninvasive alternative to routine catheterization during follow-up of HTx recipients to
B. Merkely and P. Maurovich-Horvat contributed diagnose CAV.
equally to this work.

ardiac allograft vasculopathy nary wall; therefore, intravascular ultrasound

Received May 27, 2017; accepted after revision
August 16, 2017.
Based on a presentation at the European Congress of
Radiology 2017 annual meeting, Vienna, Austria.
Supported by grant NVKP-16-1-2016-0017 from the
National Research, Development, and Innovation Office
of Hungary.
1
MTA-SE Cardiovascular Imaging Research Group,
Heart  and Vascular Center, Semmelweis University,
68 Városmajor St, Budapest H-1122, Hungary.
Address correspondence to P. Maurovich-Horvat
(p.maurovich.horvat@mail.harvard.edu).
2
Department of Cardiology, Gottsegen György National
Cardiology Institute, Budapest, Hungary.
AJR 2018; 210:314–319
0361–803X/18/2102–314
© American Roentgen Ray Society
C
(CAV) is the leading cause of
death during the first year after
heart transplantation (HTx). The
overall frequency of CAV at 1, 5, and 10 years
after transplantation is 8%, 30%, and 50%, re-
spectively [1]. CAV is characterized by dif-
fuse concentric intimal hyperplasia [2]. Be-
cause of the denervated transplanted hearts,
patients do not experience symptoms related
to ischemia; therefore, early diagnosis of
CAV is challenging. International guidelines
recommend annual or biannual invasive cor-
onary angiography for the assessment of cor-
onary status. However, invasive coronary an-
giography has limited diagnostic accuracy to
detect CAV because of the diffuse and con-
centric manifestation of the disease. Further-
more, invasive coronary angiography does
not provide information regarding the coro-
or optical coherence tomography is suggested
as a complementary imaging test [3]. The
combination of invasive coronary angiogra-
phy with intravascular imaging techniques
increases sensitivity, but their routine use in-
creases costs and rates of procedural compli-
cations; therefore, it is considered optional for
CAV assessment [4]. In addition, the Interna-
tional Society for Heart and Lung Transplan-
tation consensus statement does not recom-
mend the routine use of intravascular
ultrasound for CAV assessment [3].
Coronary CT angiography (CTA) allows
noninvasive visualization of the coronary ar-
tery wall and lumen with a high diagnostic
accuracy [5, 6]. It can detect 1.5–2 times more
coronary segments with coronary atheroscle-
rotic plaques than does invasive coronary an-
giography [7]. Notably, the absence of para-

314 AJR:210, February 2018

 Quality of Coronary CTA Images of HTx Recipients

sympathetic and sympathetic innervation of

HTx recipients (n = 50) Institutional cardiac CT registry (n ≈ 2500) the transplanted hearts results in higher rest-
ing heart rates (HRs), which may compro-
mise the diagnostic performance of coronary
Matching criteria:
• HR (± 2 beat/min) CTA. Moreover, because of their higher HRs,
• Data acquisition phase retrospective ECG-gating has been used for
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(systole/diastole) HTx recipients, which results in higher ra-

• Coronary dominance
• BMI (± 10%) diation dose. These concerns precluded the
• Sex widespread use of coronary CTA in HTx re-
• Age (± 10%) cipients [8]. Prospectively ECG-triggered
coronary CTA would be desirable because of
Control group (n = 50) its low radiation dose, but it requires a low
HR (generally < 65 beats/min). The HTx re-
cipients have higher but steady HR with min-
Study population (n = 100)
imal HR variability because of the lack of au-
tonomic innervation. The steady HR of HTx
recipients might provide a unique opportuni-
Fig. 1—Flowchart of study population selection. BMI = body mass index (weight in kilograms divided by the ty to scan these patients with low radiation
square of height in meters), HR = heart rate, HTx = heart transplantation. dose and achieve good image quality. There-

Fig. 2—Examples of 4-point Likert scale of motion artifacts in heart transplant recipients: 0, excellent image quality with no artifacts (62-year-old man); 1, good image
quality with minor artifacts (60-year-old woman); 2, moderate image quality, acceptable for routine clinical diagnosis (44-year-old woman); 3, not evaluable, with severe
artifacts impairing accurate evaluation (60-year-old man). Upper panels show cross-sectional CT angiography images of right coronary arteries with different motion
artifact severities. Lower panels show same vessels in curved multiplanar reconstructions. Arrows indicate motion artifacts.

AJR:210, February 2018 315


100
80
Coronary Segments
Percentage of
60
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40
20
0 and maximum intensity projections to evaluate
HTx Control
Recipients Subjects
fore, our aim was to assess the image qual-
ity of low-dose prospectively ECG-triggered
coronary CTA in HTx recipients.
Materials and Methods
In a retrospective matched case-control cohort
study, we evaluated the image quality of coronary
CTA performed of HTx recipients. The institutional
review board of Semmelweis University approved
the study (approval number SE-TUKEB 173/2016),
and because of the retrospective study design, in-
formed consent was waived. The study was con-
ducted in compliance with the Helsinki declaration.
During a 4-year period, 97 coronary CTAs were
performed of 57 HTx recipients to rule out CAV. If
a patient underwent more than one scan, the scan
obtained with the highest HR was selected. Scans
with breathing artifacts (n = 3), contrast agent ex-
travasation (n = 1), and high image noise or insuf-
ficient contrast opacification (n = 3) were excluded
from the study. In total, 50 HTx recipients (HTx
group) were included in the study. The image qual-
ity of the scans of the HTx recipients was com-
pared with that of scans of a control group of pa-
tients who did not undergo HTx. The control group
was selected from our institutional cardiac CT reg-
istry. We selected the control group according to
matching criteria that may influence image qual-
ity: age, sex, body mass index (weight in kilograms
divided by the square of height in meters), HR,
data acquisition phase (systole or diastole), and
coronary dominance (Fig. 1). For the HR, a maxi-
mum difference of ± 2 beats/min was allowed; for
body mass index and age, a maximum difference
of ±  10% was allowed. In addition, we matched ev-
ery pair for coronary dominance. Codominant cor-
onary system was regarded as left dominant.
All patients underwent imaging with a 256-
MDCT scanner (Brilliance iCT 256, Philips
Healthcare). Tube voltage was 100–120 kV, and
the tube current was set to 100–300 mA depend-
ing on the body mass index of the patients. Colli-
mation was 2 × 128 × 0.625 mm, with a gantry ro-
tation time of 270 ms. Both the HTx recipients and
316 AJR:210, February 2018
Bartykowszki et al.
Fig. 3—Proportions before the image acquisition. Images were recon-
of coronary segments structed with 0.8-mm slice thickness and 0.4-mm
with nondiagnostic,
moderate, good, and increment using a hybrid iterative reconstruction
excellent image quality (iDOSE 4, Philips Healthcare) technique.
Nondiagnostic in heart transplantation Reconstructed images were evaluated by two
Moderate (HTx) recipients and
readers (with 5 and 3 years of experience in coro-
Good control subjects.
Excellent nary CTA) using the 18-segment model of the Soci-
ety of Cardiovascular CT [11]. Coronary segments
with a diameter greater than 1.5 mm were assessed.
We used axial images, multiplanar reformations,
the image quality. Motion artifacts were described
in every coronary segment using a 4-point Likert
scale: 0, excellent image quality with no artifacts;
the control group were scanned with a prospec- 1, good image quality with minor artifacts; 2, mod-
tively ECG-triggered acquisition mode. When the erate image quality, acceptable for routine clini-
HR was over 80 beats/min, systolic triggering was cal diagnosis; and 3, not evaluable, with severe ar-
used at 40% of the cardiac cycle with 3% padding tifacts impairing accurate evaluation [12, 13] (Fig.
(37–43% of the R-R interval); in all other cases, 2). To quantify the total amount of motion artifacts
diastolic triggering was used at 78% of the cardiac on a per-patient level, we defined the segment mo-
cycle with 3% padding (75–81% of the R-R inter- tion score, which describes how many segments
val) [9]. We used a four-phase contrast injection had motion artifact, and the segment Likert score,
protocol with iodinated contrast agent (iomep- which is the sum of the motion severity Likert score
rol, 400 mg I/mL; Iomeron 400, Bracco), with of the patient. Because the number of coronary seg-
a flow rate of 4.5–5.5 mL/s with an extra saline ments affects the total obtainable score, we normal-
bolus preceding the contrast bolus [10]. A bolus- ized the scores by dividing them by the number of
tracking technique was used with an ROI in the segments present, which resulted in the segment
left atrium. For HR control, we used 7.5–15 mg motion score index and segment Likert score in-
ivabradine (Procorolan, 5 mg, Les Laboratoires dex. To describe how many nondiagnostic seg-
Servier) administered 3 hours before the scan in ments were present, we defined the segment nondi-
90% of HTx recipients and 50–100 mg oral meto- agnostic score and also divided it by the number of
prolol and 5–20 mg IV metoprolol (Betaloc, 1 the evaluated segments, which yielded the segment
mg/mL, AstraZeneca; 5-mg ampoule) in 58% and nondiagnostic score index. Furthermore, to assess
48% of control subjects, respectively. All patients the effect of systolic versus diastolic triggering, we
received 0.8 mg of sublingual nitroglycerin (Ni- conducted a subgroup analysis among both HTx re-
tromint, 8 mg/g, EGIS) a maximum of 1 minute cipients and control subjects.
A B
Fig. 4—Coronary CT angiograms of heart transplant recipient and age- and sex-matched control subject.
A, 48-year-old male heart transplant recipient with heart rate of 75 beats/min. No motion artifact is visible in
right coronary artery (RCA; arrow) on curved multiplanar reconstruction. Ao = aorta.
B, 48-year-old man with heart rate of 75 beats/min who did not receive heart transplant. Motion artifact (arrow)
is visible in proximal segment of RCA on curved multiplanar reconstruction. LV = left ventricle.
 Quality of Coronary CTA Images of HTx Recipients
The Shapiro-Wilk test was used to assess nor-
mality. Because all continuous variables showed
nonnormal distribution, continuous variables are
expressed as median and interquartile range (IQR).
Categoric variables are expressed as numbers and
percentages. The Mann-Whitney U test was used to
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compare continuous data of the HTx and non-HTx
groups. Categoric data were compared using the
chi-square test. Intrareader and interreader repro-
ducibility was assessed on the basis of 20 random-
ly selected individuals’ images using Cohen kappa,
interpreted as follows: 1.00–0.81, excellent; 0.80–
0.61, good; 0.60–0.41, moderate; 0.40–0.21, fair;
and 0.20–0.00, poor [14, 15]. All statistical calcu-
lations were done using SPSS software (version 23,
IBM). A p < 0.05 was considered significant.
Results
In total, 50 HTx recipients were includ-
ed in our study. Every HTx recipient had a
matched control subject who did not un-
dergo HTx; therefore, 100 subjects in total
were evaluated. In the HTx group (11 wom-
en [22%]; 4.3 years after transplantation), the
median age was 57.9 years (IQR, 46.7–59.9
years) and the median HR was 74.0 beats/
min (IQR, 67.8–79.3 beats/min), compared
with 73.0 beats/min (IQR, 68.5–80.0 beats/
min) in the matched control group (p = 0.58).
We found no significant difference between
the HTx and control groups regarding anthro-
pometric data and scan characteristics (Table
1). The effective radiation dose was relative-
ly low in both groups (3.7 mSv [IQR, 2.4–
4.3 mSv] in the HTx group vs 4.3 mSv [IQR,
2.6–4.3 mSv] in the control group; p = 0.24).
In total, 1270 coronary segments were
evaluated, 662 segments in the HTx group
and 608 segments in the control group. The
distribution of motion scores between the
two groups is shown in Figure 3. In the
HTx group, more segments (624; 94.3%)
had diagnostic image quality compared with
the control group (504; 82.9%) (p < 0.001)
(Fig. 4). In the HTx group, more segments
had excellent image quality than in the con-
trol group (442 [66.7%] vs 271 [4.5%]; p <
0.001). Furthermore, in the HTx group the
number of nondiagnostic segments was ap-
proximately one-third of that of the control
group (38 [5.8%] vs 104 [17.1%]; p < 0.001).
We a found a significant difference be-
tween the two groups regarding the seg-
ment Likert score, the segment motion score,
and the segment nondiagnostic score index-
es. The segment Likert score index of the
HTx group was approximately half that of
the control group (0.4 [IQR, 0.1–0.9] vs 0.9
AJR:210, February 2018 317
TABLE 1: Clinical Characteristics of Study Subjects
Parameters
Age (y)
Body mass indexa
Diastolic triggering, no. (%) of patients
Tube voltage (kV)
Tube current (mA)
Effective dose (mSv)
Contrast agent (mL)
Heart rate (beats/min)
Coronary dominance, no. (%) of patients
Right dominant
Left dominant
Note—Except where noted otherwise, data are median (interquartile range).
aWeight in kilograms divided by the square of height in meters.
[IQR, 0.3–1.6]; p = 0.003). Similarly, a near-
ly twofold difference was found between the
HTx and control groups regarding segment
motion score index (0.3 [IQR, 0.1–0.5] vs 0.6
[IQR, 0.2–0.9]; p = 0.001). The segment non-
diagnostic score index was lower in the HTx
group than in the control group (0.0 [IQR,
0.0–0.1] vs 0.1 [IQR, 0.0–0.3]; p = 0.004).
The image quality was better in HTx recip-
ients than in control subjects in the subgroup
with systolic triggering. This was reflected by
the difference in the segment Likert score in-
dex, which was significantly lower in the HTx
group than in the control group (0.5 [IQR,
0.4–0.7] vs 0.8 [IQR, 0.8–0.9]; p < 0.001).
Furthermore, among scans with systolic trig-
gering, we found significantly fewer motion
artifacts and more diagnostic segments in the
HTx group; their segment motion score in-
dex was almost half that of the control group
(0.8 [IQR, 0.5–1.1] vs 1.5 [IQR, 1.3–2.1]; p <
0.001), whereas their segment nondiagnos-
tic score index was almost one-fourth that of
the control group (0.07 [IQR, 0.0–0.1] vs 0.3
[IQR, 0.1–0.5]; p = 0.001).
Among diastolic images, significantly bet-
ter image quality was observed in the HTx
scans compared with the non-HTx scans; the
segment Likert score index was significantly
lower in the HTx group compared with the
non-HTx group (0.1 [IQR, 0.0–0.3] vs 0.4
[IQR, 0.1–0.6]; p = 0.03). However, among
scans with diastolic triggering, the degree
of motion and the number of nondiagnostic
segments did not differ significantly between
the HTx recipients and control subjects (seg-
ment motion score index, 0.1 [IQR, 0.0–0.4]
vs 0.5 [IQR, 0.1–1.1], p = 0.05; segment non-
Heart Transplant Control Subjects
Recipients (n = 50) (n = 50) p
57.9 (46.7–59.9) 58.6 (48.5–62.1) 0.32
25.0 (22.6–26.5) 25.0 (23.1–28.4) 0.45
31 (62.0) 31 (62.0) 1.00
120.0 (100.0–120.0) 120.0 (100.0–120.0) 0.63
300.0 (250.0–300.0) 300.0 (300.0–300.0) 0.14
3.7 (2.4–4.3) 4.3 (2.6–4.3) 0.24
90.0 (90.0–95.0) 90.0 (90.0–95.0) 0.62
74.0 (67.8–79.3) 73.0 (68.5–80.0) 0.58
0.91
39 (78.0) 39 (78.0)
11 (22.0) 11 (22.0)
diagnostic score index, 0.0 [IQR, 0.0–0.1] vs
0.0 [IQR, 0.0–0.1], p = 0.20). The median HR
with systolic triggering was 78.0 beats/min
for HTx recipients compared with 80.0 beats/
min for control subjects (p = 0.86); the me-
dian HR with diastolic triggering was 69.0
beats/min in HTx recipients compared with
70.0 beats/min in control subjects (p = 0.96).
Intrareader and interreader agreement for
image quality scores was good (κ = 0.72 and
κ = 0.62, respectively). Dichotomization of
image quality scores to excellent and non-
excellent image quality scores resulted in
excellent intrareader (κ = 0.83) and good
interreader (κ = 0.69) reproducibility. Di-
chotomization to diagnostic and nondiag-
nostic image quality scores also showed
excellent intrareader (κ = 0.82) and good in-
terreader (κ = 0.73) reproducibility.
Discussion
In this retrospective matched case-control
study, we found that scans of HTx recipients
had better coronary CTA image quality than
did scans of a matched control group with
similar HRs. Despite the relatively high HR
of HTx recipients, the number of nondiag-
nostic segments was low (5.8%), suggesting
that coronary CTA with prospective ECG-
triggering is a robust diagnostic tool with
low radiation dose in this patient population.
The subgroup analysis comparing the im-
age quality of the two groups among scans
with systolic and diastolic triggering showed
similar results. The HTx recipients had bet-
ter overall image quality compared with the
control subjects both with systolic and dia-
stolic triggering. However, the segment mo-

tion score index did not show any difference
between the two groups among the scans
triggered in diastole, which is most probably
due to the lower HR of patients undergoing
coronary CTA with diastolic triggering.
CAV is among the top three causes of death
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1 year after HTx. Invasive coronary angiog-
raphy is considered the reference standard
method to diagnose CAV. However, it has
been found that diagnosis based on a single
invasive coronary angiography is challenging
because of the concentric intimal hyperpla-
sia; furthermore, the interobserver variation
is high [16]. Numerous studies investigat-
ed the diagnostic performance of coronary
CTA to identify CAV [17–23]. von Ziegler et
al. [19] studied 26 consecutive patients with
a mean (± SD) HR of 86 ± 13 beats/min us-
ing 64-MDCT. They found that 81.4% of the
segments had diagnostic image quality. Ac-
cording to their results, coronary CTA has
high negative predictive value (99.7%), and
they concluded that coronary CTA is a reli-
able diagnostic tool to rule out CAV in HTx
recipients [19]. Similar results were shown by
Mittal et al. [17], who evaluated 130 HTx re-
cipients (mean HR, 82.7 ± 4 beats/min) with
64-MDCT. Most of the evaluated segments
(98%) had diagnostic image quality. They
concluded that coronary CTA has high sen-
sitivity, specificity, and excellent negative
predictive value for the diagnosis of CAV in
HTx recipients in comparison with invasive
angiography [17]. A meta-analysis published
by Wever-Pinzon et al. [24] showed that the
combined overall weighted mean sensitivity,
specificity, positive predictive value, and neg-
ative predictive value of CT for detection of
CAV were 97%, 81%, 78%, and 97%, respec-
tively. Importantly, these studies used retro-
spective ECG-gating, because of the higher
resting HR of HTx recipients, which result-
ed in higher radiation dose (10.2–17.5 mSv)
[17, 22, 23]. The reduction of radiation dose is
of utmost importance for HTx recipients who
undergo repeated scans and take immuno-
suppressant therapy, which substantially in-
creases cancer risk.
We found that HTx recipients can be
scanned with a prospective ECG-triggering
scan mode with a low radiation dose (mean
effective radiation dose, 3.7 mSv). Further-
more, we found that scans of HTx recipi-
ents with median HR of 74.0 beats/min have
significantly better image quality than scans
of control subjects with a similar HR (73.0
beats/min). In addition, the number of seg-
ments with excellent image quality was high-
318 AJR:210, February 2018
Bartykowszki et al.
er for HTx recipients than for control sub-
jects. In accordance with these results, the
ratio of nondiagnostic segments was lower
among HTx recipients.
Our observations might be explained by
the loss of autonomous neural control. The
surgical denervation after heart transplan-
tation causes chronotropic incompetence,
which results in elevated resting HR and
nearly absent HR variability [25–27]. Ac-
cording to Stolzmann et al. [28] and Bro-
doefel et al. [29], HR variability has a
significant effect on the image quality in pro-
spectively triggered coronary CTA. There-
fore, the lack of autonomous neural control
and the consequent regular and steady HR
seems to be optimal for prospectively ECG-
triggered coronary CTA.
Despite the excellent diagnostic accuracy
and low radiation dose of modern CT scan-
ners, the routine use of coronary CTA for
follow-up of HTx recipients has not become
widely accepted in daily practice. The guide-
lines of the International Society for Heart
and Lung Transplantation [3] and the rec-
ommendations of the European Association
of Cardiovascular Imaging and Cardiovas-
cular Imaging Department of the Brazilian
Society of Cardiology [8] raise concerns re-
garding the higher HR (higher than the op-
timal 65 beats/min) of HTx recipients and
the excess ionizing radiation. However, con-
temporary scanner technology allows coro-
nary imaging at ever decreasing radiation
doses, and, with modern scanners, the radia-
tion dose generally does not exceed that as-
sociated with invasive coronary angiography
[30, 31]. Therefore, we believe that, in expe-
rienced centers with contemporary CT scan-
ners, coronary CTA is a promising alterna-
tive to invasive coronary angiography for
follow-up of HTx recipients.
This study has some limitations that we
have to acknowledge. First, coronary seg-
ments with a diameter smaller than 1.5 mm
were excluded from the study because of the
limited accuracy of coronary CTA in dis-
tal coronary segments and small-caliber
side braches. Nevertheless, the evaluation
of small coronary segments remains a chal-
lenge even with invasive techniques.
Second, because of the specific postopera-
tive appearance of the extracardiac structures
(e.g., sternal sutures and great vessel anasto-
moses) of HTx recipients, the readers could
not be blinded to the compared groups (HTx
recipients vs control subjects), which might
represent a potential bias that affects quality
rating. Furthermore, we acknowledge that this
study was a single-center single-vendor study
using a 256-MDCT scanner, which might
limit the generalizability of our findings.
In conclusion, coronary CTA of HTx re-
cipients had significantly better image quality
compared with a control group with similar
HRs. This finding suggests that invasive coro-
nary angiography could be replaced by coro-
nary CTA in experienced centers to diagnose
CAV. In addition, a higher optimal HR thresh-
old might be recommended for coronary CTA
among HTx recipients because of the lack of
autonomous innervation of the heart and di-
minished HR variability. With the use of cor-
onary CTA in the clinical routine, the burden
of invasive investigations could be reduced in
this vulnerable patient population.
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